Environmental deformations dynamically shift human spatial memory

Place and grid cells in the hippocampal formation are commonly thought to support a unified and coherent cognitive map of space. This mapping mechanism faces a challenge when a navigator is placed in a familiar environment that has been deformed from its original shape. Under such circumstances, many transformations could plausibly serve to map a navigator's familiar cognitive map to the deformed space. Previous empirical results indicate that the firing fields of rodent place and grid cells stretch or compress in a manner that approximately matches the environmental deformation, and human spatial memory exhibits similar distortions. These effects have been interpreted as evidence that reshaping a familiar environment elicits an analogously reshaped cognitive map. However, recent work has suggested an alternative explanation, whereby deformation-induced distortions of the grid code are attributable to a mechanism that dynamically anchors grid fields to the most recently experienced boundary, thus causing history-dependent shifts in grid phase. This interpretation raises the possibility that human spatial memory will exhibit similar history-dependent dynamics. To test this prediction, we taught participants the locations of objects in a virtual environment and then probed their memory for these locations in deformed versions of this environment. Across three experiments with variable access to visual and vestibular cues, we observed the predicted pattern, whereby the remembered locations of objects were shifted from trial to trial depending on the boundary of origin of the participant's movement trajectory. These results provide evidence for a dynamic anchoring mechanism that governs both neuronal firing and spatial memory.